Design principles for energy transfer in the photosystem II supercomplex from kinetic transition networks

Yang, Shiun-Jr; Wales, David J.; Woods, Esmae J.; Fleming, Graham R.

doi:10.1038/s41467-024-53138-z

Title: Design principles for energy transfer in the photosystem II supercomplex from kinetic transition networks

Journal Article · 08 October 2024 · Nature Communications

DOI: https://doi.org/10.1038/s41467-024-53138-z · OSTI ID:2461627

^[1];

^[2];

^[1]

University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Kavli Energy NanoScience Institute, Berkeley, CA (United States)
Univ. of Cambridge (United Kingdom)

Photosystem II (PSII) has the unique ability to perform water-splitting. With light-harvesting complexes, it forms the PSII supercomplex (PSII-SC) which is a functional unit that can perform efficient energy conversion, as well as photoprotection, allowing photosynthetic organisms to adapt to the naturally fluctuating sunlight intensity. Achieving these functions requires a collaborative energy transfer network between all subunits of the PSII-SC. In this work, we perform kinetic analyses and characterise the energy landscape of the PSII-SC with a structure-based energy transfer model. With first passage time analyses and kinetic Monte Carlo simulations, we are able to map out the overall energy transfer network. We also investigate how energy transfer pathways are affected when individual protein complexes are removed from the network, revealing the functional roles of the subunits of the PSII-SC. In addition, we provide a quantitative description of the flat energy landscape of the PSII-SC. We show that it is a unique landscape that produces multiple kinetically relevant pathways, corresponding to a high pathway entropy. These design principles are crucial for balancing efficient energy conversion and photoprotection.

View Journal Article

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: Engineering and Physical Sciences Research Council (EPSRC); USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2461627

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 15; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (75)

Energy Landscapes for Proteins: From Single Funnels to Multifunctional Systems Röder, Konstantin; Joseph, Jerelle A.; Husic, Brooke E. Advanced Theory and Simulations, Vol. 2, Issue 4 https://doi.org/10.1002/adts.201800175	journal	January 2019
Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria Demmig-Adams, Barbara; Garab, Gyozo; Adams III, William Advances in Photosynthesis and Respiration https://doi.org/10.1007/978-94-017-9032-1	book	January 2014
Thermodynamic Formalism for Systems with Markov Dynamics Lecomte, V.; Appert-Rolland, C.; van Wijland, F. Journal of Statistical Physics, Vol. 127, Issue 1 https://doi.org/10.1007/s10955-006-9254-0	journal	January 2007
Structure-based simulation of linear optical spectra of the CP43 core antenna of photosystem II Müh, Frank; Madjet, Mohamed El-Amine; Renger, Thomas Photosynthesis Research, Vol. 111, Issue 1-2 https://doi.org/10.1007/s11120-011-9675-8	journal	August 2011
A study of Photosystem II fluorescence emission in terms of the antenna chlorophyll-protein complexes Jennings, Robert C.; Garlaschi, Flavio M.; Bassi, Roberto Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1183, Issue 1 https://doi.org/10.1016/0005-2728(93)90018-B	journal	November 1993
A new algorithm for Monte Carlo simulation of Ising spin systems Bortz, A. B.; Kalos, M. H.; Lebowitz, J. L. Journal of Computational Physics, Vol. 17, Issue 1 https://doi.org/10.1016/0021-9991(75)90060-1	journal	January 1975
Energy Transfer in Light-Harvesting Complexes LHCII and CP29 of Spinach Studied with Three Pulse Echo Peak Shift and Transient Grating Salverda, Jante M.; Vengris, Mikas; Krueger, Brent P. Biophysical Journal, Vol. 84, Issue 1 https://doi.org/10.1016/S0006-3495(03)74865-6	journal	January 2003
Determination of the excitation migration time in Photosystem II Broess, Koen; Trinkunas, Gediminas; van Hoek, Arie Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1777, Issue 5 https://doi.org/10.1016/j.bbabio.2008.02.003	journal	May 2008
Mechanism and regulation of the violaxanthin cycle: The role of antenna proteins and membrane lipids Jahns, Peter; Latowski, Dariusz; Strzalka, Kazimierz Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 1 https://doi.org/10.1016/j.bbabio.2008.09.013	journal	January 2009
High-light vs. low-light: Effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana Kouřil, Roman; Wientjes, Emilie; Bultema, Jelle B. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 3 https://doi.org/10.1016/j.bbabio.2012.12.003	journal	March 2013
Disturbed excitation energy transfer in Arabidopsis thaliana mutants lacking minor antenna complexes of photosystem II Dall'Osto, Luca; Ünlü, Caner; Cazzaniga, Stefano Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 12 https://doi.org/10.1016/j.bbabio.2014.09.011	journal	December 2014
Dynamic reorganization of photosystem II supercomplexes in response to variations in light intensities Albanese, Pascal; Manfredi, Marcello; Meneghesso, Andrea Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 10 https://doi.org/10.1016/j.bbabio.2016.06.011	journal	October 2016
The causes of altered chlorophyll fluorescence quenching induction in the Arabidopsis mutant lacking all minor antenna complexes Townsend, Alexandra J.; Saccon, Francesco; Giovagnetti, Vasco Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1859, Issue 9 https://doi.org/10.1016/j.bbabio.2018.03.005	journal	September 2018
Design principles of solar light harvesting in plants: Functional architecture of the monomeric antenna CP29 Mascoli, Vincenzo; Novoderezhkin, Vladimir; Liguori, Nicoletta Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 3 https://doi.org/10.1016/j.bbabio.2020.148156	journal	March 2020
The energy transfer model of nonphotochemical quenching: Lessons from the minor CP29 antenna complex of plants Lapillo, Margherita; Cignoni, Edoardo; Cupellini, Lorenzo Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 11 https://doi.org/10.1016/j.bbabio.2020.148282	journal	November 2020
Effect of Antenna-Depletion in Photosystem II on Excitation Energy Transfer in Arabidopsis thaliana van Oort, Bart; Alberts, Marieke; de Bianchi, Silvia Biophysical Journal, Vol. 98, Issue 5 https://doi.org/10.1016/j.bpj.2009.11.012	journal	March 2010
Excitation Energy Transfer and Trapping in Higher Plant Photosystem II Complexes with Different Antenna Sizes Caffarri, Stefano; Broess, Koen; Croce, Roberta Biophysical Journal, Vol. 100, Issue 9 https://doi.org/10.1016/j.bpj.2011.03.049	journal	May 2011
Capturing the Quenching Mechanism of Light-Harvesting Complexes of Plants by Zooming in on the Ensemble Mascoli, Vincenzo; Liguori, Nicoletta; Xu, Pengqi Chem, Vol. 5, Issue 11 https://doi.org/10.1016/j.chempr.2019.08.002	journal	November 2019
Transition networks for modeling the kinetics of conformational change in macromolecules Noé, Frank; Fischer, Stefan Current Opinion in Structural Biology, Vol. 18, Issue 2 https://doi.org/10.1016/j.sbi.2008.01.008	journal	April 2008
Energy landscapes: some new horizons Wales, David J. Current Opinion in Structural Biology, Vol. 20, Issue 1 https://doi.org/10.1016/j.sbi.2009.12.011	journal	February 2010
Bidirectional Energy Flow in the Photosystem II Supercomplex Leonardo, Cristina; Yang, Shiun-Jr; Orcutt, Kaydren The Journal of Physical Chemistry B, Vol. 128, Issue 33 https://doi.org/10.1021/acs.jpcb.4c02508	journal	August 2024
Evolved Minimal Frustration in Multifunctional Biomolecules Röder, Konstantin; Wales, David J. The Journal of Physical Chemistry B, Vol. 122, Issue 49 https://doi.org/10.1021/acs.jpcb.8b03632	journal	May 2018
Ultrafast Excitation Energy Transfer Dynamics in the LHCII–CP29–CP24 Subdomain of Plant Photosystem II Do, Thanh Nhut; Nguyen, Hoang Long; Akhtar, Parveen The Journal of Physical Chemistry Letters, Vol. 13, Issue 19 https://doi.org/10.1021/acs.jpclett.2c00194	journal	May 2022
Dynamical Signatures of Multifunnel Energy Landscapes Wales, David J. The Journal of Physical Chemistry Letters, Vol. 13, Issue 27 https://doi.org/10.1021/acs.jpclett.2c01258	journal	July 2022
On the Mechanism of Polaritonic Rate Suppression from Quantum Transition Paths Anderson, Michelle C.; Woods, Esmae J.; Fay, Thomas P. The Journal of Physical Chemistry Letters, Vol. 14, Issue 30 https://doi.org/10.1021/acs.jpclett.3c01188	journal	July 2023
Observation of Electronic Excitation Transfer Through Light Harvesting Complex II Using Two-Dimensional Electronic–Vibrational Spectroscopy Lewis, Nicholas H. C.; Gruenke, Natalie L.; Oliver, Thomas A. A. The Journal of Physical Chemistry Letters, Vol. 7, Issue 20 https://doi.org/10.1021/acs.jpclett.6b02280	journal	October 2016
Distribution of the chlorophyll spectral forms in the chlorophyll-protein complexes of photosystem II antenna Jennings, Robert C.; Bassi, Roberto; Garlaschi, Flavio M. Biochemistry, Vol. 32, Issue 13 https://doi.org/10.1021/bi00064a002	journal	April 1993
Photosystem II Does Not Possess a Simple Excitation Energy Funnel: Time-Resolved Fluorescence Spectroscopy Meets Theory Shibata, Yutaka; Nishi, Shunsuke; Kawakami, Keisuke Journal of the American Chemical Society, Vol. 135, Issue 18 https://doi.org/10.1021/ja312586p	journal	April 2013
A Structure-Based Model of Energy Transfer Reveals the Principles of Light Harvesting in Photosystem II Supercomplexes Bennett, Doran I. G.; Amarnath, Kapil; Fleming, Graham R. Journal of the American Chemical Society, Vol. 135, Issue 24 https://doi.org/10.1021/ja403685a	journal	June 2013
Light Harvesting in a Fluctuating Antenna Chmeliov, Jevgenij; Trinkunas, Gediminas; van Amerongen, Herbert Journal of the American Chemical Society, Vol. 136, Issue 25 https://doi.org/10.1021/ja5027858	journal	June 2014
Light Harvesting in Photosystem II Core Complexes Is Limited by the Transfer to the Trap: Can the Core Complex Turn into a Photoprotective Mode? Raszewski, Grzegorz; Renger, Thomas Journal of the American Chemical Society, Vol. 130, Issue 13 https://doi.org/10.1021/ja7099826	journal	April 2008
Femtosecond Visible/Visible and Visible/Mid-IR Pump−Probe Study of the Photosystem II Core Antenna Complex CP47 Groot, Marie Louise; Breton, Jacques; van Wilderen, Luuk J. G. W. The Journal of Physical Chemistry B, Vol. 108, Issue 23 https://doi.org/10.1021/jp037966s	journal	June 2004
Intermolecular Coulomb Couplings from Ab Initio Electrostatic Potentials: Application to Optical Transitions of Strongly Coupled Pigments in Photosynthetic Antennae and Reaction Centers Madjet, M. E.; Abdurahman, A.; Renger, T. The Journal of Physical Chemistry B, Vol. 110, Issue 34 https://doi.org/10.1021/jp0615398	journal	August 2006
Potential Energy and Free Energy Landscapes Wales, David J.; Bogdan, Tetyana V. The Journal of Physical Chemistry B, Vol. 110, Issue 42 https://doi.org/10.1021/jp0680544	journal	October 2006
Charge Separation is Virtually Irreversible in Photosystem II Core Complexes with Oxidized Primary Quinone Acceptor van der Weij−de Wit, C. D.; Dekker, J. P.; van Grondelle, R. The Journal of Physical Chemistry A, Vol. 115, Issue 16 https://doi.org/10.1021/jp1083746	journal	April 2011
Archetypal energy landscapes Wales, David J.; Miller, Mark A.; Walsh, Tiffany R. Nature, Vol. 394, Issue 6695 https://doi.org/10.1038/29487	journal	August 1998
The nature of carotenoid S* state and its role in the nonphotochemical quenching of plants Accomasso, Davide; Londi, Giacomo; Cupellini, Lorenzo Nature Communications, Vol. 15, Issue 1 https://doi.org/10.1038/s41467-024-45090-9	journal	January 2024
Disentangling the sites of non-photochemical quenching in vascular plants Nicol, Lauren; Nawrocki, Wojciech J.; Croce, Roberta Nature Plants, Vol. 5, Issue 11 https://doi.org/10.1038/s41477-019-0526-5	journal	October 2019
Identification of a pigment cluster catalysing fast photoprotective quenching response in CP29 Guardini, Zeno; Bressan, Mauro; Caferri, Roberto Nature Plants, Vol. 6, Issue 3 https://doi.org/10.1038/s41477-020-0612-8	journal	March 2020
Separating single- from multi-particle dynamics in nonlinear spectroscopy Malý, Pavel; Lüttig, Julian; Rose, Peter A. Nature, Vol. 616, Issue 7956 https://doi.org/10.1038/s41586-023-05846-7	journal	March 2023
Ultrafast energy transfer within the photosystem II core complex Pan, Jie; Gelzinis, Andrius; Chorošajev, Vladimir Physical Chemistry Chemical Physics, Vol. 19, Issue 23 https://doi.org/10.1039/C7CP01673E	journal	January 2017
A theoretical study on the dynamics of light harvesting in the dimeric photosystem II core complex: regulation and robustness of energy transfer pathways Hsieh, Shou-Ting; Zhang, Lu; Ye, De-Wei Faraday Discussions, Vol. 216 https://doi.org/10.1039/C8FD00205C	journal	January 2019
Analysis and interpretation of first passage time distributions featuring rare events Woods, Esmae J.; Wales, David J. Physical Chemistry Chemical Physics, Vol. 26, Issue 3 https://doi.org/10.1039/D3CP04199A	journal	January 2024
Intra- and inter-monomeric transfers in the light harvesting LHCII complex: the Redfield–Förster picture Novoderezhkin, Vladimir; Marin, Alessandro; van Grondelle, Rienk Physical Chemistry Chemical Physics, Vol. 13, Issue 38 https://doi.org/10.1039/c1cp21079c	journal	January 2011
Energy landscapes for diffusion: Analysis of cage-breaking processes de Souza, Vanessa K.; Wales, David J. The Journal of Chemical Physics, Vol. 129, Issue 16 https://doi.org/10.1063/1.2992128	journal	October 2008
Connectivity in the potential energy landscape for binary Lennard-Jones systems de Souza, Vanessa K.; Wales, David J. The Journal of Chemical Physics, Vol. 130, Issue 19 https://doi.org/10.1063/1.3131690	journal	May 2009
Theoretical foundations of dynamical Monte Carlo simulations Fichthorn, Kristen A.; Weinberg, W. H. The Journal of Chemical Physics, Vol. 95, Issue 2 https://doi.org/10.1063/1.461138	journal	July 1991
The topology of multidimensional potential energy surfaces: Theory and application to peptide structure and kinetics Becker, Oren M.; Karplus, Martin The Journal of Chemical Physics, Vol. 106, Issue 4 https://doi.org/10.1063/1.473299	journal	January 1997
Structural relaxation in Morse clusters: Energy landscapes Miller, Mark A.; Doye, Jonathan P. K.; Wales, David J. The Journal of Chemical Physics, Vol. 110, Issue 1 https://doi.org/10.1063/1.478067	journal	January 1999
The double-funnel energy landscape of the 38-atom Lennard-Jones cluster Doye, Jonathan P. K.; Miller, Mark A.; Wales, David J. The Journal of Chemical Physics, Vol. 110, Issue 14 https://doi.org/10.1063/1.478595	journal	April 1999
Nonequilibrium phase coexistence and criticality near the second explosion limit of hydrogen combustion Newcomb, Lucas B.; Alaghemandi, Mohammad; Green, Jason R. The Journal of Chemical Physics, Vol. 147, Issue 3 https://doi.org/10.1063/1.4994265	journal	July 2017
Molecular mechanisms of light harvesting in the minor antenna CP29 in near-native membrane lipidic environment Sardar, Samim; Caferri, Roberto; Camargo, Franco V. A. The Journal of Chemical Physics, Vol. 156, Issue 20 https://doi.org/10.1063/5.0087898	journal	May 2022
Excited-state dynamics in photosystem II: Insights from the x-ray crystal structure Vasil'ev, S.; Orth, P.; Zouni, A. Proceedings of the National Academy of Sciences, Vol. 98, Issue 15 https://doi.org/10.1073/pnas.141239598	journal	July 2001
Chlorophyll–carotenoid excitation energy transfer and charge transfer in Nannochloropsis oceanica for the regulation of photosynthesis Park, Soomin; Steen, Collin J.; Lyska, Dagmar Proceedings of the National Academy of Sciences, Vol. 116, Issue 9 https://doi.org/10.1073/pnas.1819011116	journal	February 2019
Archetypal landscapes for deep neural networks Verpoort, Philipp C.; Lee, Alpha A.; Wales, David J. Proceedings of the National Academy of Sciences, Vol. 117, Issue 36 https://doi.org/10.1073/pnas.1919995117	journal	August 2020
From antenna to reaction center: Pathways of ultrafast energy and charge transfer in photosystem II Yang, Shiun-Jr; Arsenault, Eric A.; Orcutt, Kaydren Proceedings of the National Academy of Sciences, Vol. 119, Issue 42 https://doi.org/10.1073/pnas.2208033119	journal	October 2022
Chlorophyll to zeaxanthin energy transfer in nonphotochemical quenching: An exciton annihilation-free transient absorption study Lee, Tsung-Yen; Lam, Lam; Patel-Tupper, Dhruv Proceedings of the National Academy of Sciences, Vol. 121, Issue 42 https://doi.org/10.1073/pnas.2411620121	journal	October 2024
Spin glasses and the statistical mechanics of protein folding. Bryngelson, J. D.; Wolynes, P. G. Proceedings of the National Academy of Sciences, Vol. 84, Issue 21 https://doi.org/10.1073/pnas.84.21.7524	journal	November 1987
Protein folding funnels: a kinetic approach to the sequence-structure relationship. Leopold, P. E.; Montal, M.; Onuchic, J. N. Proceedings of the National Academy of Sciences, Vol. 89, Issue 18 https://doi.org/10.1073/pnas.89.18.8721	journal	September 1992
Quenching in Arabidopsis thaliana Mutants Lacking Monomeric Antenna Proteins of Photosystem II Miloslavina, Yuliya; de Bianchi, Silvia; Dall'Osto, Luca Journal of Biological Chemistry, Vol. 286, Issue 42 https://doi.org/10.1074/jbc.M111.273227	journal	October 2011
Analysing ill-conditioned Markov chains Woods, Esmae J.; Kannan, Deepti; Sharpe, Daniel J. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 381, Issue 2250 https://doi.org/10.1098/rsta.2022.0245	journal	May 2023
Scaling concepts for the dynamics of viscous liquids near an ideal glassy state Kirkpatrick, T. R.; Thirumalai, D.; Wolynes, P. G. Physical Review A, Vol. 40, Issue 2 https://doi.org/10.1103/PhysRevA.40.1045	journal	July 1989
Classically exact overlayer dynamics: Diffusion of rhodium clusters on Rh(100) Voter, Arthur F. Physical Review B, Vol. 34, Issue 10 https://doi.org/10.1103/PhysRevB.34.6819	journal	November 1986
Stable and metastable states in mean-field Potts and structural glasses Kirkpatrick, T. R.; Wolynes, P. G. Physical Review B, Vol. 36, Issue 16 https://doi.org/10.1103/PhysRevB.36.8552	journal	December 1987
Non-Photochemical Quenching. A Response to Excess Light Energy Müller, Patricia; Li, Xiao-Ping; Niyogi, Krishna K. Plant Physiology, Vol. 125, Issue 4 https://doi.org/10.1104/pp.125.4.1558	journal	April 2001
Minor Antenna Proteins CP24 and CP26 Affect the Interactions between Photosystem II Subunits and the Electron Transport Rate in Grana Membranes of Arabidopsis de Bianchi, Silvia; Dall'Osto, Luca; Tognon, Giuseppe The Plant Cell, Vol. 20, Issue 4 https://doi.org/10.1105/tpc.107.055749	journal	April 2008
Arabidopsis Mutants Deleted in the Light-Harvesting Protein Lhcb4 Have a Disrupted Photosystem II Macrostructure and Are Defective in Photoprotection de Bianchi, Silvia; Betterle, Nico; Kouril, Roman The Plant Cell, Vol. 23, Issue 7 https://doi.org/10.1105/tpc.111.087320	journal	July 2011
Light‐harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Goral, Tomasz K.; Johnson, Matthew P.; Duffy, Christopher D. P. The Plant Journal, Vol. 69, Issue 2 https://doi.org/10.1111/j.1365-313X.2011.04790.x	journal	October 2011
Structure and assembly mechanism of plant C ₂ S ₂ M ₂ -type PSII-LHCII supercomplex Su, Xiaodong; Ma, Jun; Wei, Xuepeng Science, Vol. 357, Issue 6353 https://doi.org/10.1126/science.aan0327	journal	August 2017
Exploring Energy Landscapes Wales, David J. Annual Review of Physical Chemistry, Vol. 69, Issue 1 https://doi.org/10.1146/annurev-physchem-050317-021219	journal	April 2018
Exploring the Free Energy Landscape: From Dynamics to Networks and Back Prada-Gracia, Diego; Gómez-Gardeñes, Jesús; Echenique, Pablo PLoS Computational Biology, Vol. 5, Issue 6 https://doi.org/10.1371/journal.pcbi.1000415	journal	June 2009
Theory of Optical Spectra of Photosystem II Reaction Centers: Location of the Triplet State and the Identity of the Primary Electron Donor Raszewski, Grzegorz; Saenger, Wolfram; Renger, Thomas Biophysical Journal, Vol. 88, Issue 2 https://doi.org/10.1529/biophysj.104.050294	journal	February 2005
Excitation Energy Transfer and Charge Separation in Photosystem II Membranes Revisited Broess, Koen; Trinkunas, Gediminas; van der Weij-de Wit, Chantal D. Biophysical Journal, Vol. 91, Issue 10 https://doi.org/10.1529/biophysj.106.085068	journal	November 2006
Charge Separation and Energy Transfer in the Photosystem II Core Complex Studied by Femtosecond Midinfrared Spectroscopy Pawlowicz, N. P.; Groot, M. -L.; van Stokkum, I. H. M. Biophysical Journal, Vol. 93, Issue 8 https://doi.org/10.1529/biophysj.107.105452	journal	October 2007
Entropy crises in glasses and random heteropolymers Wolynes, P. G. Journal of Research of the National Institute of Standards and Technology, Vol. 102, Issue 2 https://doi.org/10.6028/jres.102.014	journal	March 1997

Similar Records

Entropy is an important design principle in the photosystem II supercomplex

Journal Article · 2025 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:2565894

Hall, Johanna L.; Yang, Shiun-Jr; Limmer, David T.; +1 more

Atomic Force Microscopy of Photosystem II and Its Unit Cell Clustering Quantitatively Delineate the Mesoscale Variability in Arabidopsis Thylakoids

Journal Article · 2014 · PLoS ONE · OSTI ID:1407241

Onoa, Bibiana; Schneider, Anna R.; Brooks, Matthew D.; +5 more

Probing exciton diffusion dynamics in photosynthetic supercomplexes via exciton–exciton annihilation

Journal Article · 2025 · Journal of Chemical Physics · OSTI ID:2562695

Zhang, Kunyan; Lee, Tsung-Yen; Yang, Shiun-Jr; +3 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Design principles for energy transfer in the photosystem II supercomplex from kinetic transition networks

Citation Formats

References (75)

Similar Records

Related Subjects